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General Environmental Heterogeneity As the Explanation Of bioRxiv preprint doi: https://doi.org/10.1101/141317; this version posted May 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 General environmental heterogeneity as the 2 explanation of sexuality? Comparative 3 study shows that ancient asexual taxa are 4 associated with both biotically and 5 abiotically homogeneous environments 6 7 Authors 8 Jan Toman*, Jaroslav Flegr 9 J. Toman, J. Flegr: Laboratory of Evolutionary Biology, Department of Philosophy and History 10 of Sciences, Faculty of Science, Charles University in Prague, Vinicna 7, 128 00 Prague 2, 11 Czech Republic 12 J. Toman: Tel.: +(420)221951821. Email: [email protected] 13 J. Flegr: Tel.: +(420)221951821. Email: [email protected] 14 * Corresponding author 1 bioRxiv preprint doi: https://doi.org/10.1101/141317; this version posted May 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 15 Abstract 16 Ecological theories of sexual reproduction assume that sexuality is advantageous in certain 17 conditions, for example, in biotically or abiotically more heterogeneous environments. Such 18 theories thus could be tested by comparative studies. However, the published results of these 19 studies are rather unconvincing. Here we present the results of a new comparative study based 20 solely on the ancient asexual clades. The association with biotically or abiotically homogeneous 21 environments in these asexual clades was compared with the same association in their sister, or 22 closely related, sexual clades. Using the conservative definition of ancient asexuals (i.e. age > 1 23 million years), we found six pairs for which relevant ecological data are available. The difference 24 between the homogeneity type of environment associated with the sexual and asexual species 25 was then compared in an exact binomial test. Based on available literature, the results showed 26 that the vast majority of ancient asexual clades tend to be associated with biotically or 27 abiotically, biotically, and abiotically more homogeneous environments than their sexual 28 controls. In the exploratory part of the study, we found that the ancient asexuals often have 29 durable resting stages, enabling life in subjectively homogeneous environments, live in the 30 absence of intense biotic interactions, and are very often sedentary, inhabiting benthos and soil. 31 The consequences of these findings for the ecological theories of sexual reproduction are 32 discussed. 33 KEYWORDS: ancient asexuals – asexual reproduction – Frozen evolution theory – habitat 34 heterogeneity – sexual reproduction 2 bioRxiv preprint doi: https://doi.org/10.1101/141317; this version posted May 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 35 Introduction 36 Paradox of sexual reproduction 37 The term “sexual” may be assigned to a broad array of processes (see e.g. Redfield, 2001; 38 Birky, 2009; Gorelick & Carpinone, 2009; Schön et al., 2009a). On the other hand, sex in its 39 strict sense (i.e. amphimixis) is defined as the alternation of meiosis and syngamy (Butlin et al., 40 1998a). 41 Sexual reproduction (sensu amphimixis) is one of the most enigmatic phenomena in 42 evolutionary biology, especially if its overwhelming predominance in eukaryotes is taken into 43 account (see e.g. Williams, 1975; Maynard Smith, 1978; Bell, 1982; Meirmans & Strand, 2010). 44 The reason is that it brings many obvious disadvantages in comparison to asexual reproduction— 45 the well-known two-fold cost of sex being only the first and most obvious one (see e.g. Lehtonen 46 et al., 2012). Thus, an asexual lineage invading the sexual population would be expected to 47 quickly drive its sexual conspecifics extinct (Maynard Smith, 1978). None of these 48 disadvantages apply to all sexual species because of the highly variable nature of their 49 reproduction. But, under many circumstances, the disadvantages apply profoundly (Lehtonen et 50 al., 2012). Thus, sexual reproduction remains an enigma that calls for explanation. 51 Theories of sexual reproduction 52 Many main concepts and their countless variants were proposed to explain the paradox of 53 sexual reproduction (reviewed e.g. in Williams, 1975; Maynard Smith, 1978; Bell, 1982, 1985; 54 Kondrashov, 1993; Meirmans & Strand, 2010). The genetic advantages of sexual reproduction as 55 the explanation for the maintenance of sexual reproduction are highlighted by theories like the 56 Weismann’s idea of sex generating variability, later delimited as the concept of Vicar of Bray 57 (Bell, 1982), Fisher-Muller’s accelerated evolution of sexual species (Muller, 1932; Fisher, 58 2003), breaking free of neighbouring deleterious mutations (Crow, 1970), reduction of the spread 59 of genomic parasites (Sterrer, 2002), advantage of diploidy (Lewis & Wolpert, 1979), repair of 60 DNA (Bernstein & Bernstein, 2013), restoration of epigenetic signals (Gorelick & Carpinone, 61 2009), eventually stochastic and deterministic variants of Muller’s ratchet hypothesis (Muller, 62 1964; Kondrashov, 1982). 63 Ecological theories of sexual reproduction, on the other hand, stress the assumption that 64 sex provides some ecological advantage to sexual species. Certain trends can be clearly found in 3 bioRxiv preprint doi: https://doi.org/10.1101/141317; this version posted May 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 65 the geographic distribution of sexual reproduction, as was recently summarized by Hörandl 66 (2006, 2009) or Vrijenhoek & Parker (2009). As most advantages of sexual reproduction 67 postulated by genetic theories could be achieved by automixis (Gorelick & Carpinone, 2009; 68 Neiman & Schwander, 2011), the correct answer to the “greatest paradox of evolutionary 69 biology” probably lies in the group of ecological theories of sexual reproduction, or at least in 70 some form of theoretical synthesis that includes them (West et al., 1999). 71 Ecological theories of sexual reproduction and their predictions 72 Ecological theories such as Red Queen theory (Hamilton et al., 1990), evolutionary arm- 73 races hypothesis (Dawkins & Krebs, 1979), and the fast-sexual-response hypothesis of Maynard 74 Smith (1993) emphasize the sexually reproducing organisms’ advantage when interacting with 75 other organisms, which are able to dynamically react in a co-evolutionary manner. According to 76 these “biotic heterogeneity advantage” theories, sexual species should prosper in spatially and 77 temporally biotically heterogeneous environments, i.e. environments with many biotic 78 interactions from competitors, predators, and parasites – e.g. tropical rainforests, low-latitude 79 coral reefs, ancient lakes, climax communities, or generally species-rich ecosystems In such 80 environments, selective pressures affecting the offspring differ profoundly from those that 81 affected the parents because of the coadaptation (or rather counter-adaptation) between 82 interacting organisms. In the presence of such intensive biotic interactions, sexual species would 83 be especially favoured because they maintain high genetic polymorphism and could quickly react 84 to the countermoves of their evolutionary opponents by a simple change of allele frequencies in 85 the population. The speed, not the depth, of adaptation is essential in these environments 86 (Maynard Smith, 1993). 87 Another group of ecological theories of sexual reproduction sees the main advantage of 88 sexual reproduction in the higher fitness sexual individuals or species have in abiotically 89 heterogeneous environments. This group of “abiotic heterogeneity advantage” theories 90 comprises, for example, the lottery and Sisyphean genotypes hypothesis (Williams, 1975), elbow 91 room hypothesis (Maynard Smith, 1978), tangled bank hypothesis (Bell, 1982), hypothesis of 92 fluctuating selection (Smith, 1980), and hypothesis of reduced response to fluctuating selection 93 (Roughgarden, 1991). Such environments are abiotically very variable in space and/or time, i.e. 94 diverse, unpredictable, and with unequally distributed resources – e.g. temporary or ephemeral 95 habitats, exposed habitats, dynamically changing freshwater environments, coastal habitats or 4 bioRxiv preprint doi: https://doi.org/10.1101/141317; this version posted May 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 96 more generally biomes of high latitudes and/or altitudes. The offspring usually inhabit an 97 environment different from that of their parents due to the dispersal in time and/or space. An 98 abiotic environment does not co-evolutionarily react to the evolutionary moves of its inhabitants,
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